Timothy D. Weaver

Neandertal birth canal shape and the evolution of human childbirth

Childbirth is complicated in humans relative to other primates. Unlike the situation in great apes, human neonates are about the same size as the birth canal, making passage difficult. The birth mechanism (the series of rotations that the neonate must undergo to successfully negotiate its mothers birth canal) distinguishes humans not only from great apes, but also from lesser apes and monkeys. Tracing the evolution of human childbirth is difficult, because the pelvic skeleton, which forms the margins of the birth canal, tends to survive poorly in the fossil record. Only 3 female individuals preserve fairly complete birth canals, and they all date to earlier phases of human evolution. Here we present a virtual reconstruction of a female Neandertal pelvis from Tabun, Israel. The size of Tabuns reconstructed birth canal indicates that childbirth was about as difficult in Neandertals as in present-day humans, but the canals shape indicates that Neandertals had a more primitive birth mechanism. A significant shift in childbirth apparently occurred quite late in human evolution, during the last few hundred thousand years. Such a late shift underscores the uniqueness of human childbirth and the divergent evolutionary trajectories of Neandertals and the lineage leading to present-day humans.

The shape of the Neandertal femur is primarily the consequence of a hyperpolar body form.

Neandertal femora are distinct from contemporaneous near-modern human femora. Traditionally, these contrasts in femoral shape have been explained as the result of the elevated activity levels and limited cultural abilities of Neandertals. More recently, however, researchers have realized that many of these femoral differences may be explained by the cold-adapted bodies of Neandertals vs. the warm-adapted bodies of near-modern humans. This study explicitly tests this proposed link between climate-induced body proportions and femoral shape by considering the entire hip as a unit by using geometric morphometric methods adapted to deal with articulated structures. Based on recent human patterns of variation, most contrasts in shape between the femora of Neandertals and near-modern humans seem to be secondary consequences of differences in climate-induced body proportions. These results, considered in light of hip mechanics during growth, highlight the importance of developmental and functional integration in determining skeletal form.

Close correspondence between quantitative- and molecular-genetic divergence times for Neandertals and modern humans

Recent research has shown that genetic drift may have produced many cranial differences between Neandertals and modern humans. If this is the case, then it should be possible to estimate population genetic parameters from Neandertal and modern human cranial measurements in a manner analogous to how estimates are made from DNA sequences. Building on previous work in evolutionary quantitative genetics and on microsatellites, we present a divergence time estimator for neutrally evolving morphological measurements. We then apply this estimator to 37 standard cranial measurements collected on 2,524 modern humans from 30 globally distributed populations and 20 Neandertal specimens. We calculate that the lineages leading to Neandertals and modern humans split ≈311,000 (95% C.I.: 182,000 to 466,000) or 435,000 (95% C.I.: 308,000 to 592,000) years ago, depending on assumptions about changes in within-population variation. These dates are quite similar to those recently derived from ancient Neandertal and extant human DNA sequences. Close correspondence between cranial and DNA-sequence results implies that both datasets largely, although not necessarily exclusively, reflect neutral divergence, causing them to track population history or phylogeny rather than the action of diversifying natural selection. The cranial dataset covers only aspects of cranial anatomy that can be readily quantified with standard osteometric tools, so future research will be needed to determine whether these results are representative. Nonetheless, for the measurements we consider here, we find no conflict between molecules and morphology.

The meaning of Neandertal skeletal morphology

A procedure is outlined for distinguishing among competing hypotheses for fossil morphology and then used to evaluate current views on the meaning of Neandertal skeletal morphology. Three explanations have dominated debates about the meaning of Neandertal cranial features: climatic adaptation, anterior dental loading, and genetic drift. Neither climatic adaptation nor anterior dental loading are well supported, but genetic drift is consistent with the available evidence. Climatic adaptation and activity patterns are the most discussed explanations for Neandertal postcranial features. Robust empirical relationships between climate and body form in extant humans and other endotherms currently make climatic adaptation the most plausible explanation for the wide bodies and relatively short limbs of Neandertals, and many additional postcranial features are likely secondary consequences of these overall skeletal proportions. Activity patterns may explain certain Neandertal postcranial features, but unlike the situation for climate, relationships in extant humans between morphology and activities are typically not well established. For both the cranium and the postcranium, changes in diet or activity patterns may underlie why Neandertals and Pleistocene modern humans tend to be more robust than Holocene humans.

Reliability of cranial morphology in reconstructing Neanderthal phylogeny

The usefulness of cranial morphology in reconstructing the phylogeny of closely related taxa is often questioned due to the possibility of convergence or parallelism and epigenetic response to the environment. However, it has been suggested that different cranial regions preserve phylogenetic information differentially. Some parts of the face and neurocranium are thought to be relatively developmentally flexible, and therefore to be subject to the epigenetic influence of the environment. Other parts are thought to be particularly responsive to selection for adaptation to local climate. The basicranium, on the other hand, and in particular the temporal bone, is thought to be largely genetically determined and has been argued to preserve a strong phylogenetic signal with little possibility of homoplasy. Here we test the hypotheses that cranial morphology is related to population history among recent humans, and that different cranial regions reflect population history and local climate differentially. Morphological distances among ten recent human populations were calculated from the face, vault and temporal bone using three-dimensional geometric morphometrics methods. The distance matrices obtained were then compared to neutral genetic distances and to climatic differences among the same or closely matched groups. Results indicated a stronger relationship of the shape of the vault and the temporal bone with neutral genetic distances, and a stronger association of facial shape with climate. Vault and temporal bone centroid sizes were associated with climate and particularly temperature; facial centroid size was associated with genetic distances. Temporal bone shape was more successful in tracking older population history than vault shape. Of the three cranial regions, it is therefore most appropriate for phylogenetic reconstructions among fossil humans. Analysis of temporal bone shape of both recent and Middle-Late Pleistocene humans showed Neanderthals to be morphologically very distant from both recent and fossil modern humans, indicating that Neanderthals represent a distinct evolutionary lineage.

The affinity of the dental remains from Obi-Rakhmat Grotto, Uzbekistan

A human partial maxillary dentition and a fragmentary cranium were recovered from Obi-Rakhmat Grotto in northeastern Uzbekistan in 2003. Initial descriptions of this single juvenile (OR-1) from a Middle Paleolithic archaeological context have emphasized its mosaic morphological pattern; the dentition appears archaic, while certain morphological aspects of the cranial fragments may be more ambiguous. The present study provides a systematic and comparative analysis of the dental morphology and morphometrics of OR-1 to provide a more refined appraisal of its phenetic affinity vis á vis Neandertals and modern humans. Two analyses were performed. The first uses 28 non-metric dental traits scored from Neandertals, Upper Paleolithic, and Middle Paleolithic modern humans to assess the posterior probability of group membership for the Obi-Rakhmat individual. The second is a morphometric analysis of the first upper molar of OR-1. The results of both analyses suggest the dentition of OR-1 is essentially Neandertal.

The abundance of eland, buffalo, and wild pigs in Middle and Later Stone Age sites.

Klein (1979, 1994) reported a contrast in ungulate species frequencies between the Middle Stone Age (MSA) layers of Klasies River Main (KRM) and the Later Stone Age (LSA) layers of nearby Nelson Bay Cave (NBC), South Africa. Early European travelers noted that the distinctive subtropical broadleaf forest surrounding both coastal sites housed exceptional numbers of buffalo (Syncerus caffer) and bushpig (Potamochoerus larvatus; Skead, 1980). They failed to mention eland, suggesting that eland were locally absent or rare, in keeping with this species’ tendency to avoid forest (Skinner and Chimimba, 2005). At both KRM and NBC the deposits formed under similar climatic conditions (Last Interglacial and the Holocene Interglacial, respectively), yet only the NBC LSA fauna anticipated the historic forest fauna in the abundance of buffalo and bushpig and the rarity of eland. The unanticipated abundance of eland in the KRM MSA fauna led Klein to suggest that the KRM people were less competent hunters. Unlike buffalo and bushpig, which commonly counterattack predators, eland tend to flee, and associated artifacts suggest that only the NBC LSA hunters had projectile weapons that would have allowed them to hunt dangerous species from a relatively safe distance. The NBC LSA people could then have obtained buffalo and bushpig more in proportion to their live abundance. Lacking projectiles, the KRM MSA people would have tended to capture more of the less threatening eland, which they could have driven over nearby cliffs. Driving could explain why the KRM eland were mainly prime-age adults, whereas the KRM buffalo were mostly very young or old individuals, as would be expected if the hunters focused on the most vulnerable buffalo or acquired them by scavenging. Conceivably, culture was irrelevant, and topography or some other strictly local factor explains the abundance of eland at KRM. However, a test for this would require additional fossiliferous MSA sites in the same forest, and KRM remains the only one. The KRM/ NBC contrast is roughly replicated between Die Kelders Cave 1 (DK1) and nearby Byneskranskop 1 (BNK1), where eland dominate buffalo and bushpig in the DK1MSA layers and buffalo and bushpig dominate eland in the BNK1 LSA layers (Klein and Cruz-Uribe, 1996). However, DK1 and BNK1 are located 400e500 km east of KRM and NBC (Fig. 1) in a scrub/thicket mosaic where buffalo and bushpig may not have outnumbered eland historically. In addition, the DK1 and BNK1 faunas accumulated under differing climatic conditions (mainly glacial and interglacial, respectively), and a paleoenvironmental difference could thus explain the faunal contrast. The DK1/BNK1 contrast underscores the need to control for environment before invoking cultural or human behavioral explanations for differences between sites. With Klein’s interpretation of the KRM/NBC contrast in mind, Faith (2008) undertook log-transformed regressions of eland and buffaloþ pig abundance on the total number of ungulates in 95 LSA samples and 27 MSA samples from Lesotho and South Africa. He concluded that “eland, buffalo, andwild pig are equally abundant in the MSA and LSA” (p. 24) and therefore that MSA and LSA people were equally adept hunters. We show below that Faith’s results are based on inappropriate use of regression, but even if we were to accept them, they do not show that MSA and LSA people were behaving in the same way. Eland, buffalo, and wild pigs could be equally abundant, on average, in MSA and LSA sites only if their live proportions (relative numbers) were usually the same nearby, or if MSA and LSA people, faced with different proportions at different times and places, managed to equalize the proportions in their sites. Faith’s result could mean, for example, that buffalo and pigs were generally rarer near LSA sites but that more effective LSA hunting overcame the environmental difference. Our point here is not to argue that MSA people were inferior hunters. That issue remains debatable. Rather, we are concerned with how to appropriately use the zooarchaeological record to * Corresponding author. E-mail address: rklein@stanford.edu (R.G. Klein).

Ancient DNA, late Neandertal survival, and modern-human-Neandertal genetic admixture

Fig. 1. Ancient population genetics. Although the Neandertals sample the ancient population, the living humans sample the present population. Because mtDNA lineages will be lost over time through random genetic drift, a sample from the present translates into a smaller sample of the ancient population. This makes it possible for Neandertal mtDNA lineages to have made up a large proportion of the ancient population (in this diagram 50%) but by chance not be detectable in a sample of living humans. Ancient DNA, Late Neandertal Survival, and ModernHuman–Neandertal Genetic Admixture

Variation and signatures of selection on the human face.

There has been much debate about why humans throughout the world differ in facial form. Previous studies of human skull morphology found levels of among-population differentiation that were comparable to those of neutral genetic markers, suggesting that genetic drift (neutral processes) played an important role in influencing facial differentiation. However, variation in soft-tissue morphology has not been studied in detail. In this study, we analyzed high-resolution 3D images of soft-tissue facial form in four Eurasian populations: Han Chinese, Tibetans, Uyghur and Europeans. A novel method was used to establish a high-density alignment across all of the faces, allowing facial diversity to be examined at an unprecedented resolution. These data exhibit signatures of population structure and history. However, among-population differentiation was higher for soft-tissue facial form than for genome-wide genetic loci, and high-resolution analyses reveal that the nose, brow area and cheekbones exhibit particularly strong signals of differentiation (Qst estimates: 0.3-0.8) between Europeans and Han Chinese. Our results suggest that local adaptation and/or sexual selection have been important in shaping human soft-tissue facial morphology.

Changes in human skull morphology across the agricultural transition are consistent with softer diets in preindustrial farming groups

Significance Agriculture changed not only human culture and lifeways, but human biology as well. Previous studies indicate that softer agricultural diets may have resulted in a less robust craniofacial morphology in early farmers. However, obtaining reliable estimates of worldwide subsistence effects has proved challenging. Here, we quantify changes in human skull shape and form across the agricultural transition at a global scale. Although modest, the effects are often reliably directional and most pronounced in craniofacial features that are directly involved in mastication. Agricultural foods and technologies are thought to have eased the mechanical demands of diet—how often or how hard one had to chew—in human populations worldwide. Some evidence suggests correspondingly worldwide changes in skull shape and form across the agricultural transition, although these changes have proved difficult to characterize at a global scale. Here, adapting a quantitative genetics mixed model for complex phenotypes, we quantify the influence of diet on global human skull shape and form. We detect modest directional differences between foragers and farmers. The effects are consistent with softer diets in preindustrial farming groups and are most pronounced and reliably directional when the farming class is limited to dairying populations. Diet effect magnitudes are relatively small, affirming the primary role of neutral evolutionary processes—genetic drift, mutation, and gene flow structured by population history and migrations—in shaping diversity in the human skull. The results also bring an additional perspective to the paradox of why Homo sapiens, particularly agriculturalists, appear to be relatively well suited to efficient (high-leverage) chewing.